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Cited by 240Bacterial biofilms and quorum sensingPneumonia and Respiratory InfectionsMicrobial infections and disease research

Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease

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Marks, Laura R., Davidson, Bruce A., Knight, Paul R., Hakansson, Anders P.·2013·mBio
DOI 10.1128/mbio.00438-13PMC PMC3735180
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Abstract

UNLABELLED: Streptococcus pneumoniae is a common human nasopharyngeal commensal colonizing 10% to 40% of healthy individuals, depending on age. Despite a low invasive disease rate, widespread carriage ensures that infection occurs often enough to make S. pneumoniae a leading bacterial cause of respiratory disease worldwide. However, the mechanisms behind transition from asymptomatic colonization to dissemination and disease in otherwise sterile sites remain poorly understood but are epidemiologically strongly linked to infection with respiratory viruses. In this report, we show that infection with influenza A virus and treatment with the resulting host signals (febrile-range temperatures, norepinephrine, extracytoplasmic ATP, and increased nutrient availability) induce the release of bacteria from biofilms in a newly developed biofilm model on live epithelial cells both in vitro and during in vivo colonization. These dispersed bacteria have distinct phenotypic properties different from those of both biofilm and broth-grown, planktonic bacteria, with the dispersed population showing differential virulence gene expression characteristics resulting in a significantly increased ability to disseminate and cause infection of otherwise sterile sites, such as the middle ear, lungs, and bloodstream. The results offer novel and important insights into the role of interkingdom signaling between microbe and host during biofilm dispersion and transition to acute disease. IMPORTANCE: This report addresses the mechanisms involved in transition from pneumococcal asymptomatic colonization to disease. In this study, we determined that changes in the nasopharyngeal environment result in the release of bacteria from colonizing biofilms with a gene expression and virulence phenotype different not only from that of colonizing biofilm bacteria but also from that of the broth-grown planktonic bacteria commonly used for pathogenesis studies. The work importantly also identifies specific host factors responsible for the release of bacteria and their changed phenotype. We show that these interkingdom signals are recognized by bacteria and are induced by influenza virus infection, which is epidemiologically strongly associated with transition to secondary pneumococcal disease. As virus infection is a common inducer of transition to disease among species occupying the nasopharynx, the results of this study may provide a basis for better understanding of the signals involved in the transition from colonization to disease in the human nasopharynx.

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  • Viruses impair bacterial biofilm formation and disrupt existing biofilm.

    “Viruses have also been found to impair bacterial biofilm formation and disrupt existing biofilm (141–144).”

    From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [143]

  • Bacterial growth promotion by host stress molecules is not unique to P aeruginosa and is also seen with Streptococcus pneumoniae, S aureus, and Klebsiella pneumoniae.

    “Bacterial growth promotion by host stress molecules is not unique to P aeruginosa, and is also seen with Streptococcus pneumoniae,121 S aureus,122 and Klebsiella pneumoniae.”

    From The microbiome and critical illness (2016) · cites this paper as [121]

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Authors
Marks, L. R., Davidson, B. A., Knight, P. R., & Hakansson, A. P.
Affiliations
  • University at Buffalo, State University of New York (US)
  • Buffalo VA Medical Center (US)
  • Department of Microbiology and Immunology, University at Buffalo, State University of New York, Buffalo, New York, USA
ORCID
Venue
mBio
Publisher
American Society for Microbiology
Published
2013-08-30
Volume
4
Issue
4
ISSN
  • 2150-7511 (ISSN-L)
  • 2161-2129
DOI
10.1128/mbio.00438-13
PMC
PMC3735180
OpenAlex
W2167500590
Cited by
240
References
73
Citations by year
2026: 6 · 2025: 13 · 2024: 10 · 2023: 14 · 2022: 19 · 2021: 23 · 2020: 24 · 2019: 27 · 2018: 16 · 2017: 19 · 2016: 23 · 2015: 21 · 2014: 21 · 2013: 3
FWCI
10.15
Type
journal article
Language
en
Open access
Licence
Locations
  • mBio (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Lund University Publications (Lund University) (submittedVersion)
Funders
National Heart, Lung, and Blood Institute (R01HL048889)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
  • Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
Keywords
Streptococcus pneumoniae, pneumococcal carriage, biofilm dispersal, interkingdom signaling, influenza A virus, host-pathogen interaction, virulence gene expression, norepinephrine, extracellular ATP, febrile temperature, nasopharynx, bacterioplankton
MeSH terms
Animals, Cell Line, Epithelial Cells, Humans, Mice, Inbred BALB C, Streptococcus pneumoniae, Signal Transduction, Gene Expression, Biofilms, Virulence Factors, Mice

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